Acta Physiol Plant (2016) 38:27 DOI 10.1007/s11738-015-2057-7
SHORT COMMUNICATION
Consequences of moderate drought stress on the net photosynthesis, water-use efficiency and biomass production of three poplar clones Dietmar Lu¨ttschwager1 • Dietrich Ewald2 • Lucı´a Atanet Alı´a1
Received: 21 October 2015 / Revised: 14 December 2015 / Accepted: 16 December 2015 Ó Franciszek Go´rski Institute of Plant Physiology, Polish Academy of Sciences, Krako´w 2015
Abstract The breeding of efficient but drought-tolerant poplar clones is very important for short-rotation planting because of frequent periods with low precipitation in Central Europe. Three clones exhibiting very different shoot–root ratios under well-watered conditions were investigated: (1) the aspen clone Großdubrau No. 1 (Populus tremula); (2) the newly bred aspen clone L316 9 L9 No. 21 Thermo (P. tremula 9 P. tremula); (3) and the poplar clone Max2 (P. maximowiczii 9 P. trichocarpa). All three clones were exposed to moderate drought stress. Photosynthesis and transpiration were measured. The influences of drought on the biometrical parameters of the plants were evaluated. The intrinsic water-use efficiency (WUEintrinsic) was calculated. Height growth was decreased in stressed plants. Photosynthesis and water conductivity were significantly decreased, which is why the WUEintrinsic exhibited a greater increase in Max2 than in the aspen clones. The poplar clone Max2 showed low WUE after sufficient watering, but this parameter exhibited a greater increase under drought stress compared with the aspen clones. Max2 was characterised by intensive root growth that was diminished under stress. In contrast, both aspen clones were less adaptive to moderate drought stress. The capability to change the WUEintrinsic under different water availabilities can be considered a possible selection criterion for breeding. Communicated by J. Zwiazek. & Dietmar Lu¨ttschwager
[email protected] 1
Institute of Landscape Biogeochemistry, Leibniz Centre for Agricultural Landscape Research (ZALF), Eberswalder Straße 84, 15374 Mu¨ncheberg, Germany
2
Institute of Forest Genetics, Thu¨nen-Institute, Eberswalder Chausee 3a, 15377 Waldsieversdorf, Germany
Keywords Photosynthesis Water-use efficiency Drought stress Shoot:root ratio Poplar
Introduction Planting of fast-growing tree species in short rotation helps to produce a sufficient amount of biomass for energy production in a short duration (Dillen et al. 2013). Such planting also contributes to the increased variety of species (Fry 2008; Baum et al. 2009), filtration of pollutants from air, soil and water (Licht and Isebrands 2005) and noise prevention. Poplars are of special importance in this context; however, they are among the most susceptible woody species to drought stress (Tschaplinski et al. 1994; Dreyer et al. 2004). Many poplar species are native to areas with high soil moisture; thus, they are believed to be relatively intolerant of soil moisture deficits (Demeritt 1990). Poplar growth is frequently limited by water deficits in Central Europe (Meyer et al. 2013). There is increasing concern as to whether currently used poplar clones will be able to withstand the predicted and increasingly severe and frequent drought periods (Tschaplinski et al. 2006; Ryan 2011). Anderegg et al. (2013) studied the hydraulic deterioration of aspen forests and declared that a single extreme drought event may have altered the properties of these trees up to a decade later. However, the variations in drought tolerance among and within poplar species are large (Ceulemans et al. 1988; Tschaplinski et al. 1994; Robinson and Raffa 1998; Rood et al. 2003). Therefore, the breeding of more drought-tolerant clones is necessary. To minimise these impacts of climate change, knowledge of the degree of adaptability or the vulnerability of plant species to the expected new environmental conditions is essential.
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However, what are suitable physiological performance parameters for breeding? Photosynthesis is a key phenomenon that contributes substantially to plant growth and development. The effect of drought on photosynthesis is directly attributed to stomatal limitations in the diffusion of gases, which ultimately alter photosynthesis and mesophyll metabolism (Chaves et al. 2009). Clones should have leaf gas exchange characteristics that maximise carbon gain while minimising water loss and avoiding the potentially damaging effects of drought-induced stress (Silim et al. 2009). Clones with the best ideotype will be those that exhibit continued productivity despite limiting soil moisture conditions. This characteristic can result from changes in soil moisture sensitivity, water-use efficiency (WUE) or gas exchange characteristics, among other factors. Evaluating plant growth, gas exchange and WUE under soil moisture deficit will help to identify those clones with the best ideotype and elucidate the reasons for their continued productivity under limiting soil moisture (Nash 2009). In our studies, three of eight clones that were previously investigated under well-watered conditions (Lu¨ttschwager et al. 2015) were selected because they had the most variable shoot:root ratios. We hypothesised that these clones would react to moderate drought with different physiological and morphological strategies. Examining changes in WUE should help to identify clones that can be used more extensively in breeding or genome studies.
Materials and methods Three clones were selected for a drought stress experiment: (1) poplar clone Max 2 (M); (2) aspen clone Großdubrau No. 1 (Gd); and (3) aspen clone L316 9 L9 No. 21 Thermo (LT). These clones were propagated by tissue culture (Ewald et al. 2009). Micropropagated shoot tips were kept at 23 °C under a 16-hour photoperiod illuminated by warm-white fluorescent light. When the root-induced plants first formed roots (approximately 10–20 mm long), they were transferred into a greenhouse and planted in commercial propagation soil (22.6 % carbon and 0.57 % nitrogen, pH 5.9; substrate mixture: natural clay, white peat and peat dust [Gebr. Patzer GmbH & Co. KG, SinntalJossa]) in individual 2-L pots. Soil was pressed to a standardised soil volume of 1800 cm3, resulting in a standardised dry soil density of 0.29 g/cm3. Thus, the volumetric water content (VWC) in each pot could be controlled and stabilised by weighing and selective watering. To avoid infiltration of endophytic bacteria and fungi and to increase the absorbing capacity of the roots in relation to the water and nutrient supplies, the pots were inoculated with a commercial ‘‘Myccorhizae soluble’’ powder (Mushroom Production Centre GmbH, Innsbruck,
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Austria) (Ulrich et al. 2008). Young plants were placed in a greenhouse under supplementary light, with a day length of approximately 12 h. After 12 weeks, the plants were moved to a climate chamber, where they were grown under controlled environmental conditions (21 °C, 60–65 % relative humidity and 15 °C, 85 % relative humidity during the day and night, respectively). Ten plants of each clone were selected for stress and control treatments. Two automatic watering systems (GARDENA C1030 plus) were installed in the climate chamber to ensure for the controlled watering of plants. Each plant pot was weighed twice per week and before gas exchange measurements were performed. Then, VWC was calculated. Differences were corrected by manual watering. Due to the increasing plant weights, additional correction was necessary. This correction was performed based on a linear correlation between plant fresh mass and height for each trait at the end of the experiment. The subtly differential irrigation began after plant transplantation into the soil substrate on the 88th day. Gas exchange was measured using the 1st fully expanded leaf of each plant. Measurements were initiated at 2 h after switching on the light using a portable open gas exchange system (HCM-1000, Walz, Effeltrich, Germany) at 500 lmol/m2 s PAR. The measured light responses were considered saturating intensities for all clones during the summertime (Lu¨ttschwager et al. 2015). Repetitions were carried out in darkness on the second day to estimate the respiration rate. Approximately 8 h per day from morning until afternoon (8 am to 4 pm) were required to complete the measurements for the 60 plants. To avoid systematic errors due to known diurnal variations in photosynthesis, the time sequence was planned randomly. Measurements in light were performed four times during the drought experiment on the 87th, 96th, 108th, and 122nd days after planting in the soil. Respiration was measured before the water deficit period began on the 88th day and at the end of the experiment on the 123rd day after planting in the soil. Stomatal conductance (gs) was calculated as a quotient of transpiration (E) and air-to-leaf vapour pressure deficit (VPD) at the leaf level. WUEintrinsic was calculated according to Farquhar et al. (1989) and Tambussi et al. (2007) based on net photosynthesis (A) and gs: WUEintrinsic = A/gs = VPD (A/E). One sample per leaf with an area of 12.5 mm2 was cut and frozen (-80 °C) for chlorophyll analyses. Samples were ground using quartz sand, incubated in 1 ml of 80 % acetone and calcium carbonate in the dark and cold and then centrifuged for 15 min. Chlorophyll concentrations were determined according to Lichtenthaler and Wellburn (1983) using a spectrophotometer (UV1, Thermo Electro Corporation) at 663 and 647 nm. Plant height was measured on the same days as gas exchange to determine the ontogenetic development of
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plant growth and the influence of drought stress on growth. Leaf area (LA) measurements of whole plants were limited to a subset of each trait (n = 3) to limit effort. The wholeplant-specific leaf area (SLA) was calculated from this subset as a quotient of LA and dry mass (65 °C for 14 h). Whole-plant LA was estimated using the leaf dry mass for all 60 plants and the SLA values. LAs were determined using a mobile handheld scanner (Scandoo SD, dnt-GmbH, Dietzenbach) and open-access LaForE software (V. Lehsten, Oldenburg University). All of the collected leaves that fell and those that were harvested at the end of the experiment were dried and weighed. Harvesting of the whole biomass in addition to the leaves permitted biometric analyses of the woody parts. Leaves were counted, and the basal diameters of the non-branched thin trunks were measured. The root bales were cleaned with water jets and thoroughly separated from the soil materials. The samples (wood with bark and roots) were then dried for 48 h at 105 °C and weighed. The Newman–Keuls test was performed to analyse the significance of differences, with probability levels of p = 0.05, 0.01 and below. Further data were evaluated by linear correlation analysis (Pearson coefficients). Statistical analyses were conducted using NCSS statistical software and Mathematica 8.0, distributed by Wolfram.
Results and discussion In this study, three poplar clones were exposed to drought conditions to examine whether they had the ability to adjust morphologically or to acclimate physiologically to decreased soil moisture. At the beginning of the drought experiment, the heights of the aspen plants already exceeded 1 m. Plants of poplar clone Max2 were the same age but were much smaller. This difference, however, was due to the experimental design and the chosen propagation method (tissue culture) for all plants. Control plants were maintained at approximately 45 % VWC throughout the experimental period. Small deviations and spreads in the VWCs arose in the context of the forecast biomass estimate after corrections were made due to differences in the height:biomass ratios. The VWC decreased stepwise from 45 % to approximately 15 % in all of the pots of stressed plants. The final mean VWCs in the water deficit pots were 14.1, 13.9, and 12.8 % for Gd, LT, and M, respectively. Thus, the height growth of the stressed plants decreased slightly but significantly. Over the 35 days of the drought stress experiment, stressed plants exhibited height increases compared with control plants of only 71, 76 and 72 % for the clones Gd, LT and M, respectively. However, these increases occurred under moderate stress, i.e. wilting was not
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observed in any stressed plant. Therefore, although a stress influence was already measureable, there was no obvious visual effect on plant growth. As expected, both net photosynthesis and transpiration decreased in all of the plants, along with a reduction in VWC. Many studies have reported rapid decreases in stomatal conductance and net photosynthesis with increasing soil water deficit in poplars (Schulte et al. 1987; Ceulemans et al. 1988; Bassman and Zwier 1991; Ni and Pallardy 1991; Arango-Velez et al. 2011). The decreases in our study were nearly identical for the two aspen clones. Photosynthesis and transpiration were reduced significantly in leaves under drought by 61 and 73 % in Gd and by 76 and 78 % in LT, respectively (Fig. 1). Therefore, WUEintrinsic exhibited almost no decrease (Gd) or was slightly increased (LT) in the aspen clones. Transpiration, however, decreased in the Max2 plants under drought to a much greater extent (95 %) than photosynthesis (82 %), whereas WUEintrinsic was much higher (approximately sixfold). WUE is often higher in poplar clones that have been preexposed to moisture deficit conditions (Tschaplinski et al. 1994; Liu and Dickmann 1996; Monclus et al. 2006). Drought-tolerant clones are expected to have not only a lower steady-state gs under well-watered conditions but also a higher gs and A at lower leaf water potentials and a more gradual reduction in leaf gas exchange in response to progressive drought than moderately tolerant and droughtsensitive clones (Nash 2009). A decreased gs may limit the net photosynthetic rate and transpiration with progressive drought stress, leading to increased WUE, because transpiration is inhibited more strongly than photosynthesis (Xu et al. 2010). The linear correlation (significant at a 0.1 % a level for all 60 plants together) between photosynthesis and transpiration improved steadily during the increasing drought stress: the Pearson coefficient was 0.717 at the beginning of the experiments on the 87th day after planting in the soil, and on the 96th, 108th and 122nd days, the coefficients were 0.790, 0.804 and 0.828, respectively. Furthermore, significant reductions in dark respiration due to the drought trait were observed for the clones LT and M but not for Gd. Increased chlorophyll concentrations were found for all three clones after drought stress; however, the greatest increase (one-third) was detected in Max2. This clone seemed to be able to partially counteract the effects of stomatal regulation by chlorophyll enrichment in leaves under drought. The aspen clones and Max2 also differed with regard to biomass production under drought (Table 1). Drought had no significant effect on SLA. The number of pre-fallen leaves, however, was much higher for both aspen clones compared with the poplar clone Max2, but it is important to consider the different leaf surface structures of these
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Fig. 1 Net photosynthesis (A), transpiration (E) and intrinsic wateruse efficiency (WUEintrinsic) of young, fully developed leaves of three poplar clones (Großdubrau1 [Gd], L316 9 L9 No. 21 Thermo [LT] and Max2 [M]) during a drought experiment with moderate stress:
Table 1 Biometric parameters of poplar plants at the end of the drought stress experiment
Clone
Gd
Trait
Control
drought-exposed plants are in grey, control plants are in black, and the mean values and standard deviations are shown; n = 10. The bars with different letters indicate significant differences according to the Newman–Keuls test, with p B 0.05
LT Stress
Control
M Stress
Control
Stress 6.8 (0.8)
Basal diameter (mm)
12.3 (0.7)
11.0 (0.7)
11.8 (0.6)
10.8 (0.3)
8.2 (1.2)
Leaf number
48 (3)
42 (2)
47 (5)
45 (3)
32 (4)
28 (3)
SLA (cm2/g)
266
259
250
265
181
178
Area (calc.) (cm2)
4322
3166
4029
3419
2067
1460
Pre-fallen leaves (%)
4.0
12.4
2.0
10.1
1.1
3.6
Dry weight (g) Leaves
16.2 (1.5)
12.2 (1.9)
16.1 (1.8)
12.9 (0.7)
11.4 (2.4)
8.2 (1.6)
Stems and petioles
29.4 (3.3)
22.5 (3.4)
29.0 (4.2)
23.6 (1.6)
9.6 (3.6)
6.5 (2.2)
Roots
17.0 (2.8)
14.2 (3.0)
21.7 (5.9)
16.1 (2.6)
8.7 (3.9)
4.7 (2.1)
Shoot:root ratio
2.8 (0.3)
2.6 (0.3)
2.2 (0.6)
2.4 (0.4)
2.6 (0.7)
3.5 (0.9)
Chlorophylla (mg/m2)
336 (37)
400 (108)
286 (52)
326 (70)
416 (64)
556 (65)
Mean values and standard deviations are in parentheses (n = 10). The stressed plants are significantly different from the controls in all parameters, except for SLA (all) and chlorophyll (LT), as determined by the Newman–Keuls test, with p B 0.05 a
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Measured leaves, only one leaf per clone, young, fully developed
Acta Physiol Plant (2016) 38:27
clones. The leaf surface of Max2 was waxier and, therefore, more protected than those of the aspen clones. Under water shortage, the biomasses of the aspen decreased by 20–25 % for all of the plant components. This reduction was considerably higher in the clone Max2 and primarily affected the root mass, which was reduced by half. The water deficit value and LA exhibited a smaller decrease in clone LT than in Gd and M. The numbers of pre-fallen leaves were much higher in both aspen clones compared with the poplar clone Max2. However, despite the similar ages of the plants, the aspen clones had already matured further than the poplar clone Max2 before the beginning of the drought experiment. Therefore, the absolute values of nearly all of the biometric components were very different between the aspen clones and the poplar clone Max2. The shoot:root ratio was higher (approximately onethird) in Max2 plants under water deficit compared with the controls. This value increased in the aspen clone LT by only 9 % and decreased in the clone Gd by 6 %. Under wellwatered conditions, Gd had the highest shoot:root ratio (Lu¨ttschwager et al. 2015), indicating a very effective use of resources (nutrients, water, and energy) to obtain a high growth potential of the shoot. If conditions are variable and water availability is at its lower limit, then there is no buffer within the root system itself. Gd plants react immediately to these conditions by reducing shoot growth. In contrast, Max2 plants do not exhibit such specialised behaviour and are capable, even under drought stress conditions, to perform well at the expense of reduced root growth. We used a pot volume of only 2 L. Small volumes of rooting medium may restrict plant growth (Ismail et al. 1994). However, Max2 exhibited the greatest decrease in root mass under drought, and this clone generally had a much lower root mass compared with the aspen clones. The roots of Max2 had nearly no contact with the pot walls; thus, restricted root growth was unlikely. Different strategies should result in a division between ‘‘generalists’’ and ‘‘specialists’’ (Lu¨ttschwager et al. 2015). The poplar clone Max2 showed low WUE after sufficient watering but exhibited a marked increase in this parameter under drought stress compared with the aspen clones. This clone (‘‘generalist’’) was characterised by intensive root growth that was diminished under stress. The leaves of the clone Max2 had a higher photosynthetic capability during sufficient watering compared with those of the aspen clones. However, these leaves also transpired comparatively more water. In contrast, both aspen clones (‘‘specialists’’) reacted less adaptively under moderate drought stress. In a previous experiment, the aspen clone Großdubrau1 exhibited the greatest seasonal difference in WUE under well-watered conditions. This clone had the most weakly developed root system and was, therefore, the
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least able to tolerate a short period of extreme drought (unpublished data). Silim et al. (2009) demonstrated substantial variability among nine investigated poplar clones in their abilities to regulate leaf water potential, stomatal conductance and carbon gain with decreasing soil water content. The drought-tolerant clones exhibited the greatest decreases in the leaf water potential during progressive drought, whereas those of the drought-sensitive clones remained relatively high. Comparison of the drought-tolerant clones with the drought-sensitive clones revealed that the former exhibited greater carbon allocation to roots during the early stages of drought but that the latter exhibited no plasticity of biomass allocation under water deficit (Marron et al. 2002). A study conducted in France of 29 poplar hybrids led to the discovery that most productive genotypes exhibit the lowest drought stress tolerances. However, less productive genotypes were more stable under dry conditions (Monclus et al. 2006; 2009). Attia et al. (2015) found that anisohydric genotypes grew the fastest under ample water conditions and had higher photosynthetic rates under increasing drought and that isohydric poplars had a higher WUE. They proposed three strategies to explain how closely related biomass species deal with drought stress: survival isohydric, sensitive anisohydric, and resilience anisohydric. Our experiments strongly indicate that both aspen clones use anisohydric strategies and that Max2, a widely used commercial clone, is an isohydric plant, despite the missing water potential data. Results obtained by Canadian and French working groups are in support of the use of these strategies by biomass species. Due to phenotypic plasticity, plants with identical genetic makeups (clones) from a given individual can have differences in morphology and physiology depending on the prevailing environmental conditions during their development. Acclimation, a shift in a plant’s response pattern following exposure to an environmental condition is related to the degree of plasticity possessed by the plant (Bazzaz 1991). The ability to change the WUEintrinsic under different water availabilities can be considered a possible selection criterion for breeding. However, a variety of high-performing poplar clones must be investigated to confirm this conclusion. Author contribution statement Dietmar Lu¨ttschwager designed and performed the experiment and wrote the manuscript. Dietrich Ewald selected and originated poplar clones and propagated them by tissue culture. Lucia Atanet Alia participated by experiment execution and statistical analyses. Acknowledgments This project was funded and supported by the German Federal Ministry of Food and Agriculture, Agency for Renewable Resources (FNR) under FKZ: 22012510. We thank Christine Ewald for her technical assistance.
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